Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>

ABSTRACT Geobacter sulfurreducens is a model microbe for elucidating the mechanisms for extracellular electron transfer in several biogeochemical cycles, bioelectrochemical applications, and microbial metal corrosion. Multiple lines of evidence previously suggested that electrically conductive pili...

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Autores principales:	Xinying Liu, David J. F. Walker, Stephen S. Nonnenmann, Dezhi Sun, Derek R. Lovley
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	Geobacter cytochromes electromicrobiology microbial nanowires pili Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ee1b9150aea448f49c4e60b85acd21c2
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spelling	oai:doaj.org-article:ee1b9150aea448f49c4e60b85acd21c22021-11-10T18:37:52ZDirect Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>10.1128/mBio.02209-212150-7511https://doaj.org/article/ee1b9150aea448f49c4e60b85acd21c22021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02209-21https://doaj.org/toc/2150-7511ABSTRACT Geobacter sulfurreducens is a model microbe for elucidating the mechanisms for extracellular electron transfer in several biogeochemical cycles, bioelectrochemical applications, and microbial metal corrosion. Multiple lines of evidence previously suggested that electrically conductive pili (e-pili) are an essential conduit for long-range extracellular electron transport in G. sulfurreducens. However, it has recently been reported that G. sulfurreducens does not express e-pili and that filaments comprised of multi-heme c-type cytochromes are responsible for long-range electron transport. This possibility was directly investigated by examining cells, rather than filament preparations, with atomic force microscopy. Approximately 90% of the filaments emanating from wild-type cells had a diameter (3 nm) and conductance consistent with previous reports of e-pili harvested from G. sulfurreducens or heterologously expressed in Escherichia coli from the G. sulfurreducens pilin gene. The remaining 10% of filaments had a morphology consistent with filaments comprised of the c-type cytochrome OmcS. A strain expressing a modified pilin gene designed to yield poorly conductive pili expressed 90% filaments with a 3-nm diameter, but greatly reduced conductance, further indicating that the 3-nm diameter conductive filaments in the wild-type strain were e-pili. A strain in which genes for five of the most abundant outer-surface c-type cytochromes, including OmcS, were deleted yielded only 3-nm-diameter filaments with the same conductance as in the wild type. These results demonstrate that e-pili are the most abundant conductive filaments expressed by G. sulfurreducens, consistent with previous functional studies demonstrating the need for e-pili for long-range extracellular electron transfer. IMPORTANCE Electroactive microbes have significant environmental impacts, as well as applications in bioenergy and bioremediation. The composition, function, and even existence of electrically conductive pili (e-pili) has been one of the most contentious areas of investigation in electromicrobiology, in part because e-pili offer a mechanism for long-range electron transport that does not involve the metal cofactors common in much of biological electron transport. This study demonstrates that e-pili are abundant filaments emanating from Geobacter sulfurreducens, which serves as a model for long-range extracellular electron transfer in direct interspecies electron transfer, dissimilatory metal reduction, microbe-electrode exchange, and corrosion caused by direct electron uptake from Fe(0). The methods described in this study provide a simple strategy for evaluating the distribution of conductive filaments throughout the microbial world with an approach that avoids artifactual production and/or enrichment of filaments that may not be physiologically relevant.Xinying LiuDavid J. F. WalkerStephen S. NonnenmannDezhi SunDerek R. LovleyAmerican Society for MicrobiologyarticleGeobactercytochromeselectromicrobiologymicrobial nanowirespiliMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Geobacter cytochromes electromicrobiology microbial nanowires pili Microbiology QR1-502
spellingShingle	Geobacter cytochromes electromicrobiology microbial nanowires pili Microbiology QR1-502 Xinying Liu David J. F. Walker Stephen S. Nonnenmann Dezhi Sun Derek R. Lovley Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
description	ABSTRACT Geobacter sulfurreducens is a model microbe for elucidating the mechanisms for extracellular electron transfer in several biogeochemical cycles, bioelectrochemical applications, and microbial metal corrosion. Multiple lines of evidence previously suggested that electrically conductive pili (e-pili) are an essential conduit for long-range extracellular electron transport in G. sulfurreducens. However, it has recently been reported that G. sulfurreducens does not express e-pili and that filaments comprised of multi-heme c-type cytochromes are responsible for long-range electron transport. This possibility was directly investigated by examining cells, rather than filament preparations, with atomic force microscopy. Approximately 90% of the filaments emanating from wild-type cells had a diameter (3 nm) and conductance consistent with previous reports of e-pili harvested from G. sulfurreducens or heterologously expressed in Escherichia coli from the G. sulfurreducens pilin gene. The remaining 10% of filaments had a morphology consistent with filaments comprised of the c-type cytochrome OmcS. A strain expressing a modified pilin gene designed to yield poorly conductive pili expressed 90% filaments with a 3-nm diameter, but greatly reduced conductance, further indicating that the 3-nm diameter conductive filaments in the wild-type strain were e-pili. A strain in which genes for five of the most abundant outer-surface c-type cytochromes, including OmcS, were deleted yielded only 3-nm-diameter filaments with the same conductance as in the wild type. These results demonstrate that e-pili are the most abundant conductive filaments expressed by G. sulfurreducens, consistent with previous functional studies demonstrating the need for e-pili for long-range extracellular electron transfer. IMPORTANCE Electroactive microbes have significant environmental impacts, as well as applications in bioenergy and bioremediation. The composition, function, and even existence of electrically conductive pili (e-pili) has been one of the most contentious areas of investigation in electromicrobiology, in part because e-pili offer a mechanism for long-range electron transport that does not involve the metal cofactors common in much of biological electron transport. This study demonstrates that e-pili are abundant filaments emanating from Geobacter sulfurreducens, which serves as a model for long-range extracellular electron transfer in direct interspecies electron transfer, dissimilatory metal reduction, microbe-electrode exchange, and corrosion caused by direct electron uptake from Fe(0). The methods described in this study provide a simple strategy for evaluating the distribution of conductive filaments throughout the microbial world with an approach that avoids artifactual production and/or enrichment of filaments that may not be physiologically relevant.
format	article
author	Xinying Liu David J. F. Walker Stephen S. Nonnenmann Dezhi Sun Derek R. Lovley
author_facet	Xinying Liu David J. F. Walker Stephen S. Nonnenmann Dezhi Sun Derek R. Lovley
author_sort	Xinying Liu
title	Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
title_short	Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
title_full	Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
title_fullStr	Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
title_full_unstemmed	Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>
title_sort	direct observation of electrically conductive pili emanating from <italic toggle="yes">geobacter sulfurreducens</italic>
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/ee1b9150aea448f49c4e60b85acd21c2
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Direct Observation of Electrically Conductive Pili Emanating from <italic toggle="yes">Geobacter sulfurreducens</italic>

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